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Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells
Physiological and pathological morphogenetic events involve a wide array of collective movements, suggesting that multicellular arrangements confer biochemical and biomechanical properties contributing to tissue-scale organization. The Ciona cardiopharyngeal progenitors provide the simplest model of...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8700272/ https://www.ncbi.nlm.nih.gov/pubmed/34842140 http://dx.doi.org/10.7554/eLife.70977 |
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author | Bernadskaya, Yelena Y Yue, Haicen Copos, Calina Christiaen, Lionel Mogilner, Alex |
author_facet | Bernadskaya, Yelena Y Yue, Haicen Copos, Calina Christiaen, Lionel Mogilner, Alex |
author_sort | Bernadskaya, Yelena Y |
collection | PubMed |
description | Physiological and pathological morphogenetic events involve a wide array of collective movements, suggesting that multicellular arrangements confer biochemical and biomechanical properties contributing to tissue-scale organization. The Ciona cardiopharyngeal progenitors provide the simplest model of collective cell migration, with cohesive bilateral cell pairs polarized along the leader-trailer migration path while moving between the ventral epidermis and trunk endoderm. We use the Cellular Potts Model to computationally probe the distributions of forces consistent with shapes and collective polarity of migrating cell pairs. Combining computational modeling, confocal microscopy, and molecular perturbations, we identify cardiopharyngeal progenitors as the simplest cell collective maintaining supracellular polarity with differential distributions of protrusive forces, cell-matrix adhesion, and myosin-based retraction forces along the leader-trailer axis. 4D simulations and experimental observations suggest that cell-cell communication helps establish a hierarchy to align collective polarity with the direction of migration, as observed with three or more cells in silico and in vivo. Our approach reveals emerging properties of the migrating collective: cell pairs are more persistent, migrating longer distances, and presumably with higher accuracy. Simulations suggest that cell pairs can overcome mechanical resistance of the trunk endoderm more effectively when they are polarized collectively. We propose that polarized supracellular organization of cardiopharyngeal progenitors confers emergent physical properties that determine mechanical interactions with their environment during morphogenesis. |
format | Online Article Text |
id | pubmed-8700272 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
spelling | pubmed-87002722022-01-04 Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells Bernadskaya, Yelena Y Yue, Haicen Copos, Calina Christiaen, Lionel Mogilner, Alex eLife Computational and Systems Biology Physiological and pathological morphogenetic events involve a wide array of collective movements, suggesting that multicellular arrangements confer biochemical and biomechanical properties contributing to tissue-scale organization. The Ciona cardiopharyngeal progenitors provide the simplest model of collective cell migration, with cohesive bilateral cell pairs polarized along the leader-trailer migration path while moving between the ventral epidermis and trunk endoderm. We use the Cellular Potts Model to computationally probe the distributions of forces consistent with shapes and collective polarity of migrating cell pairs. Combining computational modeling, confocal microscopy, and molecular perturbations, we identify cardiopharyngeal progenitors as the simplest cell collective maintaining supracellular polarity with differential distributions of protrusive forces, cell-matrix adhesion, and myosin-based retraction forces along the leader-trailer axis. 4D simulations and experimental observations suggest that cell-cell communication helps establish a hierarchy to align collective polarity with the direction of migration, as observed with three or more cells in silico and in vivo. Our approach reveals emerging properties of the migrating collective: cell pairs are more persistent, migrating longer distances, and presumably with higher accuracy. Simulations suggest that cell pairs can overcome mechanical resistance of the trunk endoderm more effectively when they are polarized collectively. We propose that polarized supracellular organization of cardiopharyngeal progenitors confers emergent physical properties that determine mechanical interactions with their environment during morphogenesis. eLife Sciences Publications, Ltd 2021-11-29 /pmc/articles/PMC8700272/ /pubmed/34842140 http://dx.doi.org/10.7554/eLife.70977 Text en © 2021, Bernadskaya et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited. |
spellingShingle | Computational and Systems Biology Bernadskaya, Yelena Y Yue, Haicen Copos, Calina Christiaen, Lionel Mogilner, Alex Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells |
title | Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells |
title_full | Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells |
title_fullStr | Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells |
title_full_unstemmed | Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells |
title_short | Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells |
title_sort | supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells |
topic | Computational and Systems Biology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8700272/ https://www.ncbi.nlm.nih.gov/pubmed/34842140 http://dx.doi.org/10.7554/eLife.70977 |
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